Influence of Temperature on Development of Yersinia pestis Foregut Blockage in Xenopsylla cheopis (Siphonaptera: Pulicidae) and Oropsylla montana (Siphonaptera: Ceratophyllidae)

Abstract

Abstract Plague, caused by the flea-transmitted bacterial pathogen Yersinia pestis, is primarily a disease of wild rodents distributed in temperate and tropical zones worldwide. The ability of Y. pestis to develop a biofilm blockage that obstructs the flea foregut proventriculus facilitates its efficient transmission through regurgitation into the host bite site during flea blood sucking. While it is known that temperature influences transmission, it is not well-known if blockage dynamics are similarly in accord with temperature. Here, we determine the influence of the biologically relevant temperatures, 10 and 21°C, on blockage development in flea species, Xenopsylla cheopis (Rothschild) and Oropsylla montana (Baker), respectively, characterized by geographical distribution as cosmopolitan, tropical or endemic, temperate. We find that both species exhibit delayed development of blockage at 10°C. In Y. pestis infected X. cheopis, this is accompanied by significantly lower survival rates and slightly decreased blockage rates, even though these fleas maintain similar rates of persistent infection as at 21°C. Conversely, irrespective of infection status, O. montana withstand 21 and 10°C similarly well and show significant infection rate increases and slightly greater blocking rates at 10 versus 21°C, emphasizing that cooler temperatures are favorable for Y. pestis transmission from this species. These findings assert that temperature is a relevant parameter to consider in assessing flea transmission efficiency in distinct flea species residing in diverse geographical regions that host endemic plague foci. This is important to predict behavioral dynamics of plague regarding epizootic outbreaks and enzootic maintenance and improve timeous implementation of flea control programs.